A jumbo cyanophage encodes the most comprehensive ribosomal protein set in the known virosphere

Abstract It has been proposed that a defining distinction between viruses and cells lies in the absence or presence of ribosomal genes, respectively. Recent studies revealing that viruses occasionally encode ribosomal proteins (RPs) have challenged this view. However, so far, only viral genomes with up to three RPs have been discovered. Here, we perform a functional genome analysis of the Microcystis jumbo phage PhiMa05 and show that it encodes six RPs, an RP acetyltransferase, and a ribosome biogenesis protein. To our knowledge, this makes PhiMa05 the first cyanophage reported to encode RPs, as well as the virus with the most comprehensive RP-coding set of the known virosphere. Evolutionary analyses suggest that these viral RP-coding genes may have been horizontally transferred from a temperate ancestor of PhiMa05 to certain members of the Vampirovibrionia, a non-photosynthetic basal lineage of Cyanobacteriota, via the integration of the viral genome. We find that four RPs, the RP acetyltransferase, and the ribosome biogenesis protein of the PhiMa05-like prophages are the only copies of those proteins that the near-complete genomes of some Vampirovibrio hosts possess. We hypothesize that such cellular organisms may depend on the PhiMa05-like prophage for protein synthesis, and hence life itself. Collectively, our results provide evidence for the existence of viruses with particularly enriched sets of RP-coding genes and indicate that, in some cases, such viral genes have been transferred to cells, potentially becoming essential for the survival of the host.